Embryonic oxygen enhances learning ability in hatchling lizards

Sun, Bao‐Jun; Wang, Tingting; Pike, David A.; Liang, Liang; Du, Wei‐Guo

doi:10.1186/1742-9994-11-21

Cited by 15 publications

(12 citation statements)

References 30 publications

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“…()). Altered body composition and lower growth rates are predicted from metabolic suppression because mitosis will be slowed (Douglas et al., ; Harrison et al., ), which may lead to extended incubation duration under chronic hypoxia (Sun, Wang, Pike, Liang, & Du, ). Indeed, P. muralis had lower dry mass and total energy content, suggesting that the conversion from yolk to tissue was affected by hypoxia.…”

Section: Discussionmentioning

confidence: 99%

“…However, constraints on yolk utilization, and hence hatchling size, may have important fitness consequences (Sinervo, ; Warner, ). In alligators, laboratory‐simulated hypoxia has been shown to cause a reduction in both embryonic and post‐hatching growth rates (Owerkowicz, Elsey, & Hicks, ; Crossley, & Altimiras, ) and may even compromise cognitive capacity in some hatchling lizards (Sun et al., ). As adults, reptiles are expected to cope well with high‐altitude hypoxia owing to their low basal metabolic rates (McNab, ; Jackson, ), though empirical evidence to test this generalization is lacking (Powell, & Hopkins, ).…”

Section: Discussionmentioning

confidence: 99%

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Physiological plasticity in lizard embryos exposed to high‐altitude hypoxia

et al. 2017

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Coping with novel environments may be facilitated by plastic physiological responses that enable survival during environmentally sensitive life stages. We tested the capacity for embryos of the common wall lizard (Podarcis muralis) from low altitude to cope with low-oxygen partial pressure (hypoxia) in an alpine environment. Developing embryos subjected to hypoxic atmospheric conditions (15-16% O sea-level equivalent) at 2,877 m above sea level exhibited responses common to vertebrates acclimatized to or evolutionarily adapted to high altitude: suppressed metabolism, cardiac hypertrophy, and hyperventilation. These responses might have contributed to the unaltered incubation duration and hatching success relative to the ancestral, low-altitude, condition. Even so, hypoxia constrained egg energy utilization such that larger eggs produced hatchlings with relatively low mass. These findings highlight the role of physiological plasticity in maintaining fitness-relevant phenotypes in high-altitude environments, providing impetus to further explore altitudinal limits to ecological diversification in ectothermic vertebrates.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Physiological plasticity in lizard embryos exposed to high‐altitude hypoxia

et al. 2017

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“…For example, development in hypoxia has long-term effects on post-hatching cardiovascular phenotypes in snapping turtles (Chelydra serpentina; Wearing et al, 2016Wearing et al, , 2017, decreases swimming performance in snakes (Natrix maura; F.A. and J.S., unpublished results), and impacts cognitive ability in lizards (Eremias argus; Sun et al, 2014). The adaptive significance of embryonic plasticity in response to hypoxia can only be evaluated by quantifying the long-term effects on individual fitness (Mitchell et al, 2018).…”

Section: Embryo Physiology and Developmentmentioning

confidence: 99%

“…Under certain conditions, oxygen restrictions can also result in depressed metabolism, decreased growth and reduced survivorship to hatching (Iungman and Piña, 2013;Warburton et al, 1995). These early developmental effects can persist into later life phenotypes (Sun et al, 2014;Wearing et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype

Kouyoumdjian

Gangloff

Souchet

et al. 2019

Journal of Experimental Biology

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Increased global temperatures have opened previously inhospitable habitats, such as at higher elevations. However, the reduction of oxygen partial pressure with increase in elevation represents an important physiological constraint that may limit colonization of such habitats, even if the thermal niche is appropriate. To test the mechanisms underlying the response to ecologically relevant levels of hypoxia, we performed a translocation experiment with the common wall lizard (Podarcis muralis), a widespread European lizard amenable to establishing populations outside its natural range. We investigated the impacts of hypoxia on the oxygen physiology and reproductive output of gravid common wall lizards and the subsequent development and morphology of their offspring. Lowland females transplanted to high elevations increased their haematocrit and haemoglobin concentration within days and maintained routine metabolism compared with lizards kept at native elevations. However, transplanted lizards suffered from increased reactive oxygen metabolite production near the oviposition date, suggesting a cost of reproduction at high elevation. Transplanted females and females native to different elevations did not differ in reproductive output (clutch size, egg mass, relative clutch mass or embryonic stage at oviposition) or in post-oviposition body condition. Developing embryos reduced heart rates and prolonged incubation times at high elevations within the native range and at extreme high elevations beyond the current range, but this reduced oxygen availability did not affect metabolic rate, hatching success or hatchling size. These results suggest that this opportunistic colonizer is capable of successfully responding to novel environmental constraints in these important life-history stages.

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“…Viviparous embryos maintain a relatively stable gas exchange between the mother and themselves through complex extra-embryonic membranes or placenta, whereas oviparous embryos are exposed to the external environment and may face unpredictable availability of O 2 and water (Deeming & Thompson 1991;Mess & Ferner 2010;Liang et al 2015). Identifying how embryos tolerate such unpredictability is crucial for the understanding of embryonic responses to environmental changes, because both O 2 and water availability can significantly affect embryonic development and hatchling phenotypes in oviparous vertebrates (Nechaeva 2011;Zhao et al 2013;Sun et al 2014;Bodensteiner et al 2015).…”

Section: Introductionmentioning

confidence: 99%

Reduced egg shell permeability affects embryonic development and hatchling traits in Lycodon rufozonatum and Pelodiscus sinensis

Tang

Chen

2018

Integrative Zoology

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The response of embryos to unpredictable hypoxia is critical for successful embryonic development, yet there remain significant gaps in our understanding of such responses in reptiles with different types of egg shell. We experimentally generated external regional hypoxia by sealing either the upper half or bottom half of the surface area of eggs in 2 species of reptiles (snake [Lycodon rufozonatum] with parchment egg shell and Chinese softshelled turtle [Pelodiscus sinensis] with rigid egg shell), then monitored the growth pattern of the opaque white patch in turtle eggs (a membrane that attaches the embryo to the egg shell and plays an important role in gas exchange), the embryonic heart rate, the developmental rate and the hatchling traits in turtle and snake eggs in response to external regional hypoxia. The snake embryos from the hypoxia treatments facultatively increased their heart rate during incubation, and turtle embryos from the upper-half hypoxia treatment enhanced their growth of the opaque white patch. Furthermore, the incubation period and hatching success of embryos were not affected by the hypoxia treatment in these 2 species. External regional hypoxia significantly affected embryonic yolk utilization and offspring size in the snake and turtle. Compared to sham controls, embryos from the upper-half hypoxia treatment used less energy from yolk and, therefore, developed into smaller hatchlings, but embryos from the bottom-half hypoxia treatment did not.

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Embryonic oxygen enhances learning ability in hatchling lizards

Cited by 15 publications

References 30 publications

Physiological plasticity in lizard embryos exposed to high‐altitude hypoxia

Physiological plasticity in lizard embryos exposed to high‐altitude hypoxia

Transplanting gravid lizards to high elevation alters maternal and embryonic oxygen physiology, but not reproductive success or hatchling phenotype

Reduced egg shell permeability affects embryonic development and hatchling traits in Lycodon rufozonatum and Pelodiscus sinensis

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